Abstract
Toothed whales (Odontoceti, Cetacea) are well-known for their ability to produce complex vocalizations, to use tools, to possess self-recognition, and for their extreme behavioural plasticity. The toothed whale intelligence is said to compete with that of primates, so does their extremely large brain to body size ratio. Common explanations for the acquisition of such large brains over the evolutionary time (encephalization) in toothed whales range from their demanding, complex social lives, to their feeding habits, to echolocation. Yet, several studies found no macroevolutionary trend in Odontoceti encephalization, which casts doubts on its selective advantage. We applied a recently developed phylogenetic comparative method to study macroevolutionary trends in relative brain size (RBS) and brain size evolutionary rates in cetaceans, comparing toothed whales to the other cetaceans and contrasting groups of species as ascribed to different feeding categories. We found that cetaceans as a whole followed a trend for increased encephalization over time, starting from small-brained archaeocete ancestors. Toothed whales do not show this same trend in RBS but have possessed larger RBS than any other cetacean ever since the beginning of their existence. The rate of RBS evolution in Odontoceti is significantly slower than in other Cetacea and slower than the rate of Odontoceti body size evolution. These results suggest that toothed whales’ history is characterized by high and conservative relative encephalization. Feeding lifestyle does not explain these patterns, while the appearance of echolocation within stem group Odontoceti remains a viable candidate for them.
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All data generated or analysed during this study are included in this published article and its Supplementary Information files.
References
Aiello, L. C., & Wells, J. C. (2002). Energetics and the evolution of the genus Homo. Annual Review of Anthropology, 31(1), 323–338. https://doi.org/10.1146/annurev.anthro.31.040402.085403.
Berta, A., Lanzetti, A., Ekdale, E. G., & Deméré, T. A. (2016). From teeth to baleen and raptorial to bulk filter feeding in mysticete cetaceans: The role of paleontological, genetic, and geochemical data in feeding evolution and ecology. Integrative and Comparative Biology, 56(6), 1271–1284. https://doi.org/10.1093/icb/icw128.
Berta, A., Sumach, J. L., & Kovacs, K. M. (2007). Marine mammals: Evolutionary biology (second edition). Polar Research. https://doi.org/10.3402/polar.v26i1.6210.
Bianucci, G., & Landini, W. (2002). A new short-rostrum odontocete (Mammalia: Cetacea) from the Middle Miocene of the eastern Netherlands. Beaufortia, 52(11), 187–196.
Cancho, R. F. I., & Lusseau, D. (2006). Long-term correlations in the surface behavior of dolphins. Europhysics Letters, 74(6), 1095–1101. https://doi.org/10.1209/epl/i2005-10596-9.
Castiglione, S., Serio, C., Mondanaro, A., Di Febbraro, M., Profico, A., Girardi, G., et al. (2019). Simultaneous detection of macroevolutionary patterns in phenotypic means and rate of change with and within phylogenetic trees including extinct species. PLoS ONE, 14(1), e0210101. https://doi.org/10.1371/journal.pone.0210101.
Castiglione, S., Tesone, G., Piccolo, M., Melchionna, M., Mondanaro, A., Serio, C., et al. (2018). A new method for testing evolutionary rate variation and shifts in phenotypic evolution. Methods in Ecology and Evolution, 62, 181. https://doi.org/10.1111/2041-210X.12954.
Churchill, M., Geisler, J. H., Beatty, B. L., & Goswami, A. (2018). Evolution of cranial telescoping in echolocating whales (Cetacea: Odontoceti). Evolution, 72(5), 1092–1108. https://doi.org/10.1111/evo.13480.
Clapham, P. J. (1996). The social and reproductive biology of Humpback Whales: An ecological perspective. Mammal Review, 26(1), 27–49. https://doi.org/10.1111/j.1365-2907.1996.tb00145.x.
Clementz, M. T., Goswami, A., Gingerich, P. D., & Koch, P. L. (2006). Isotopic records from early whales and sea cows: Contrasting patterns of ecological transition. Journal of Vertebrate Paleontology, 26(2), 355–370. https://doi.org/10.1671/0272-4634(2006)26[355:IRFEWA]2.0.CO;2.
Connor, R. C. (2007). Dolphin social intelligence: Complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals. Philosophical Transactions of the Royal Society B: Biological Sciences, 362(1480), 587–602. https://doi.org/10.1098/rstb.2006.1997.
DeCasien, A. R., Williams, S. A., & Higham, J. P. (2017). Primate brain size is predicted by diet but not sociality. Nature Ecology and Evolution, 1(5), 0112. https://doi.org/10.1038/s41559-017-0112.
Eisenberg, J. F., & Wilson, D. E. (1978). Relative brain size and feeding strategies in the chiroptera. Evolution, 32(4), 740–751. https://doi.org/10.1111/j.1558-5646.1978.tb04627.x.
Freckleton, R. P. (2002). On the misuse of residuals in ecology: Regression of residuals vs. multiple regression. Journal of Animal Ecology, 71(3), 542–545. https://doi.org/10.1046/j.1365-2656.2002.00618.x.
Freckleton, R. P. (2009). The seven deadly sins of comparative analysis. Journal of Evolutionary Biology, 22(7), 1367–1375. https://doi.org/10.1111/j.1420-9101.2009.01757.x.
Fordyce, R. E. (1992). Cetacean evolution and Eocene/Oligocene environments. In D. R. Prothero & W. A. Berggren (Eds.), Eocene–Oligocene climatic and biotic evolution (pp. 368–381). Princeton, NJ: Princeton University Press. https://doi.org/10.1515/9781400862924.368.
Geisler, J. H., Colbert, M. W., & Carew, J. L. (2014). A new fossil species supports an early origin for toothed whale echolocation. Nature, 508(7496), 383.
Gingerich, P. D. (2015). body weight and relative brain size (encephalization) in Eocene Archaeoceti (Cetacea). Journal of Mammalian Evolution, 23(1), 17–31. https://doi.org/10.1007/s10914-015-9304-y.
Gittleman, J. L. (1986). Carnivore brain size, behavioral ecology, and phylogeny. Journal of Mammalogy, 67(1), 23–36. https://doi.org/10.2307/1380998.
Harvey, P. H., & Pagel, M. D. (1988). The allometric approach to species differences in brain size. Human Evolution, 3(6), 461–472. https://doi.org/10.1007/BF02436332.
Herculano-Houzel, S., Catania, K., Manger, P. R., & Kaas, J. H. (2015). Mammalian brains are made of these: A dataset of the numbers and densities of neuronal and nonneuronal cells in the brain of glires, primates, scandentia, eulipotyphlans, afrotherians and artiodactyls, and their relationship with body mass. Brain, Behavior and Evolution, 86(3–4), 145–163. https://doi.org/10.1159/000437413.
Herman, L. M., Matus, D. S., Herman, E. Y. K., Ivancic, M., & Pack, A. A. (2001). The bottlenosed dolphin’s (Tursiops truncatus) understanding of gestures as symbolic representations of its body parts. Animal Learning and Behavior, 29(3), 250–264. https://doi.org/10.3758/BF03192891.
Ichishima, H., Barnes, L. G., Fordyce, R. E., Kimura, M., & Bohaska, D. J. (1994). A review of kentriodontine dolphins (Cetacea, Delphinoidea, Kentriodontidae): Systematics and biogeography. The Island Arc, 3(4), 486–492. https://doi.org/10.1111/j.1440-1738.1994.tb00127.x.
Jerison, H. J. (1985). Animal intelligence as encephalization. Philosophical Transactions of the Royal Society B: Biological Sciences, 308(1135), 21–35. https://doi.org/10.1098/rstb.1985.0007.
Johnston, C., & Berta, A. (2010). Comparative anatomy and evolutionary history of suction feeding in cetaceans. Marine Mammal Science, 27(3), 493–513. https://doi.org/10.1111/j.1748-7692.2010.00420.x.
Kratsch, C., & McHardy, A. C. (2014). RidgeRace: Ridge regression for continuous ancestral character estimation on phylogenetic trees. Bioinformatics, 30(17), i527–i533. https://doi.org/10.1093/bioinformatics/btu477.
Krützen, M., Mann, J., Heithaus, M. R., Connor, R. C., Bejder, L., & Sherwin, W. B. (2005). Cultural transmission of tool use in bottlenose dolphins. Proceedings of the National Academy of Sciences of USA, 102(25), 8939–8943. https://doi.org/10.1073/pnas.0500232102.
Lenth, R. (2018). Emmeans: Estimated marginal means, aka least-squares means. R package version, 1(1).
Lusseau, D. (2006). Why do dolphins jump? Interpreting the behavioural repertoire of bottlenose dolphins (Tursiops sp.) in Doubtful Sound, New Zealand. Behavioural Processes, 73(3), 257–265. https://doi.org/10.1016/j.beproc.2006.06.006.
Mace, G. M., Harvey, P. H., & Clutton-Brock, T. H. (2009). Brain size and ecology in small mammals. Journal of Zoology, 193(3), 333–354. https://doi.org/10.1111/j.1469-7998.1981.tb03449.x.
Manger, P. R. (2013). Questioning the interpretations of behavioral observations of cetaceans: Is there really support for a special intellectual status for this mammalian order? Neuroscience, 250, 664–696. https://doi.org/10.1016/j.neuroscience.2013.07.041.
Manger, P. R. (2006). An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain. Biological Reviews, 81(2), 293–338. https://doi.org/10.1017/S1464793106007019.
Marino, L., Connor, R. C., Fordyce, R. E., Herman, L. M., Hof, P. R., Lefebvre, L., et al. (2007). Cetaceans have complex brains for complex cognition. PLoS Biology, 5(5), e139. https://doi.org/10.1371/journal.pbio.0050139.
Marino, L. (2004). Dolphin cognition. Current Biology, 14(21), R910–R911. https://doi.org/10.1016/j.cub.2004.10.010.
Marino, L., McShea, D. W., & Uhen, M. D. (2004). Origin and evolution of large brains in toothed whales. The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology, 281(2), 1247–1255. https://doi.org/10.1002/ar.a.20128.
Marx, F. G., & Fordyce, R. E. (2015). Baleen boom and bust: A synthesis of mysticete phylogeny, diversity and disparity. Open Science, 2(4), 140434. https://doi.org/10.1098/rsos.140434.
May-Collado, L. J., Agnarsson, I., & Wartzok, D. (2007). Phylogenetic review of tonal sound production in whales in relation to sociality. BMC Evolutionary Biology, 7(1), 136. https://doi.org/10.1186/1471-2148-7-136.
McCurry, M. R., Fitzgerald, E. M. G., Evans, A. R., Adams, J. W., & McHenry, C. R. (2017). Skull shape reflects prey size niche in toothed whales. Biological Journal of the Linnean Society, 121(4), 936–946. https://doi.org/10.1093/biolinnean/blx032.
McGowen, M. R., Gatesy, J., & Wildman, D. E. (2014). Molecular evolution tracks macroevolutionary transitions in Cetacea. Trends in Ecology and Evolution, 29(6), 336–346. https://doi.org/10.1016/j.tree.2014.04.001.
Milinkovitch, M. C. (1995). Molecular phylogeny of cetaceans prompts revision of morphological transformations. Trends in Ecology and Evolution, 10(8), 328–334. https://doi.org/10.1016/S0169-5347(00)89120-X.
Montgomery, S. H., Mundy, N. I., & Barton, R. A. (2016). Brain evolution and development: Adaptation, allometry and constraint. Proceedings of the Royal Society B: Biological Sciences. https://doi.org/10.1098/rspb.2016.0433.
Montgomery, S. H., Geisler, J. H., McGowen, M. R., Fox, C., Marino, L., & Gatesy, J. (2013). The evolutionary history of cetacean brain and body size. Evolution, 67(11), 3339–3353. https://doi.org/10.1111/evo.12197.
Mortensen, H. S., Pakkenberg, B., Dam, M., Dietz, R., Sonne, C., Mikkelsen, B., et al. (2014). Quantitative relationships in delphinid neocortex. Frontiers in Neuroanatomy, 8(46), 301. https://doi.org/10.3389/fnana.2014.00132.
Navarrete, A. F., Blezer, E. L., Pagnotta, M., de Viet, E. S., Todorov, O. S., Lindenfors, P., et al. (2018). Primate brain anatomy: New volumetric MRI measurements for neuroanatomical studies. Brain, Behavior and Evolution, 91(2), 109–117. https://doi.org/10.1159/000488136.
Park, T., Fitzgerald, E. M. G., & Evans, A. R. (2016). Ultrasonic hearing and echolocation in the earliest toothed whales. Biology Letters. https://doi.org/10.1098/rsbl.2016.0060.
Perea, G., Navarrete, M., & Araque, A. (2009). Tripartite synapses: Astrocytes process and control synaptic information. Trends in Neurosciences, 32(8), 421–431. https://doi.org/10.1016/j.tins.2009.05.001.
Raia, P., Castiglione, S., Serio, C., Mondanaro, A., Melchionna, M., Di Febbraro, M., et al. (2019). RRphylo: Phylogenetic ridge regression methods for comparative studies. R package version 2.1.0. https://github.com/pasraia/RRphylo.
Reidenberg, J. S., & Laitman, J. T. (2004). Anatomy of infrasonic communication in baleen whales: Divergent mechanisms of sound generation in mysticetes and odontocetes. The Journal of the Acoustical Society of America, 115(5), 2556–2556. https://doi.org/10.1121/1.4783866.
Reiss, D., & Marino, L. (2001). Mirror self-recognition in the bottlenose dolphin: A case of cognitive convergence. Proceedings of the National Academy of Sciences of USA, 98(10), 5937–5942. https://doi.org/10.1073/pnas.101086398.
Rendell, L., & Whitehead, H. (2001). Culture in whales and dolphins. Behavioral and Brain Sciences, 24(02), 309–324. https://doi.org/10.1017/S0140525X0100396X.
Ridgway, S. H., Carlin, K. P., Van Alstyne, K. R., Hanson, A. C., & Tarpley, R. J. (2016). Comparison of dolphins’ body and brain measurements with four other groups of cetaceans reveals great diversity. Brain, Behavior and Evolution, 88(3–4), 235–257. https://doi.org/10.1159/000454797.
Shultz, S., & Dunbar, R. (2010). Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proceedings of the National Academy of Sciences of USA, 107(50), 21582–21586. https://doi.org/10.1073/pnas.1005246107.
Slater, G. J., Price, S. A., Santini, F., & Alfaro, M. E. (2010). Diversity versus disparity and the radiation of modern cetaceans. Proceedings. Biological Sciences/The Royal Society, 277(1697), 3097–3104. https://doi.org/10.1098/rspb.2010.0408.
Steeman, M. E., Hebsgaard, M. B., Fordyce, R. E., Ho, S. Y., Rabosky, D. L., Nielsen, R., et al. (2009). Radiation of extant cetaceans driven by restructuring of the oceans. Systematic Biology, 58(6), 573–585.…
Thewissen, J. G. M., Cooper, L. N., Clementz, M. T., Bajpai, S., & Tiwari, B. N. (2007). Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature, 450(7173), 1190–1194. https://doi.org/10.1038/nature06343.
Uhen, M. D. (2004). Form, function, and anatomy of Dorudon atrox (Mammalia, Cetacea): An Archaeocete from the Middle to Late Eocene of Egypt. Papers on Paleontology, 34, 1–222.
Weisbecker, V., Blomberg, S., Goldizen, A. W., Brown, M., & Fisher, D. (2015). The evolution of relative brain size in marsupials is energetically constrained but not driven by behavioral complexity. Brain, Behavior and Evolution, 85(2), 125–135. https://doi.org/10.1159/000377666.
Whiten, A. (2001). Imitation and cultural transmission in apes and cetaceans. Behavioral and Brain Sciences, 24(02), 359–360. https://doi.org/10.1017/S0140525X01603960.
Wright, A., Scadeng, M., Stec, D., Dubowitz, R., Ridgway, S., & Leger, J. S. (2017). Neuroanatomy of the killer whale (Orcinus orca): A magnetic resonance imaging investigation of structure with insights on function and evolution. Brain Structure and Function, 222(1), 417–436. https://doi.org/10.1007/s00429-016-1225-x.
Acknowledgements
We are grateful to Francesco Carotenuto for critical comments on an earlier version of the manuscript. Phil Gingerich provided some crucial data on extinct cetaceans’ brain mass estimates.
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Serio, C., Castiglione, S., Tesone, G. et al. Macroevolution of Toothed Whales Exceptional Relative Brain Size. Evol Biol 46, 332–342 (2019). https://doi.org/10.1007/s11692-019-09485-7
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DOI: https://doi.org/10.1007/s11692-019-09485-7